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Mammals can influence growth, reproduction, competitive ability, and survival of woody plants by virtue of selective browsing and gnawing of dormant shoots during winter. Apparently in response to this type of herbivory, plants have evolved chemical and mechanical deterrents to mammalian herbivores. We report on plant ontogeny and biogeography, which exert their influence on herbivory at different spatiotemporal scales. To evaluate how plant ontogeny influences herbivory, we conducted a meta-analysis of 128 studies, encompassing 37 plant and 10 mammal species, in which juvenile and mature growth stages of conspecific plants were made available to mammals during winter in temperate and northern latitudes. Mammals ate more of the mature-stage growth in 96% of the studies, and stage-specific differences in consumption were very large (d = 2.16). Plants characterized by rapid growth rates or low tolerances to resource limitation elicited the greatest degree of stage-specific discrimination by mammals, consistent with existing theories regarding tradeoffs governing plant growth and defense. The influence of a plant's growth rate and tolerance to resource limitation was dependent on climatic regime; plants grown in areas with harsh winter conditions tended to elicit greater discrimination of juvenile- and mature-stage growth by mammals than plants grown in more moderate climates. Further evidence for biogeographical variation in mammalian consumption came from 14 feeding studies, including 6 plant and 6 mammal species, that compared conspecific plants of the juvenile growth stage either grown or collected at different localities. In 86% of the studies, extent of herbivory by mammals varied inversely with latitude, and this yielded a moderate effect (Z = −0.46, r = −0.53). We discuss potential roles of life history, climate, and historical association of plants and mammals in shaping these biogeographical patterns.
Populations of 2 species of arvicoline rodents, the prairie vole (Microtus ochrogaster) and meadow vole (M. pennsylvanicus), were monitored monthly in alfalfa, bluegrass, and tallgrass prairie habitats in east-central Illinois from 1972 through 1997. Alfalfa provides very high-quality preferred food and poor vegetative cover for both vole species, whereas bluegrass provides intermediate food and vegetative cover. Preferred food resources were very low, especially for M. ochrogaster, and vegetative cover was very dense in tallgrass prairie. Maximum and mean population densities of M. ochrogaster were highest in alfalfa, intermediate in bluegrass, and lowest in tallgrass prairie. Populations of M. ochrogaster displayed synchronous 3- to 4-year multiannual cycles in all 3 habitats. Cycles were most pronounced in alfalfa, less pronounced in bluegrass, and barely discernible in tallgrass prairie. Food availability seems more important than vegetative cover for the success of M. ochrogaster. Densities of M. pennsylvanicus generally were very low in bluegrass and alfalfa habitats, both of which contained an abundance of preferred food plants. When M. pennsylvanicus was present in abundance in these 2 habitats, populations displayed annual or erratic fluctuations. Densities of M. pennsylvanicus were much higher in tallgrass prairie than in the other 2 habitats. Although vegetative cover seems more important than food availability for the success of M. pennsylvanicus, no evidence existed for population cycles in tallgrass prairie. We found no synchrony among population fluctuations of the 2 species of voles in the 3 habitats.
We conducted 2 field experiments to assess relative importance of acorn-embryo excision in the caching decisions of small mammals. In the 1st, we selectively provisioned small mammals with metal-tagged acorns of red oak (Quercus rubra) and white oak (Q. alba) at 40 point locations in 8 sites in an oak forest in northeastern Pennsylvania. We then followed the fate of cached seeds by relocating acorns with metal detectors soon after they were cached and again in spring after seeds began to germinate. At least 1 species of small mammal excised embryos of >70% of the cached acorns of white oak and <4% of those of red oak. Animals also were observed to revisit caches in spring and excise embryos of germinating acorns. More excised acorns of white oak were found intact in spring than those of red oak, indicating that the behavior is important for long-term storage of these seeds. In a 2nd experiment, we presented free-ranging Mexican gray squirrels (Sciurus aureogaster) with pairs of acorns of 5 native white oak and 5 native red oak species and recorded caching events and whether or not cached seeds had their embryos removed. Squirrels cached significantly more acorns of white oak species, frequently excised embryos of these seeds, and only excised embryos of red oaks when they were germinating. These results support our previous hypothesis that the behavior of embryo excision is geographically widespread and has important implications for cache-management strategies of some diurnal tree squirrels and their effect on dispersal of oaks.
Inventories of mammals in the Neotropics usually are derived from specimens recorded at a single site, about 25 km2 in area, but this may not represent the diversity of the whole region. To illustrate this point, presence of 42 species of nonvolant mammals was recorded in the Chiquibul Forest Reserve, an area of subtropical wet forest in the Maya Mountains of western Belize. Data on diversity and abundance of mammals at that site were compared with 3 other sites in the Maya Mountains to determine how measurements varied with location of site. Of the nonvolant species, <33% were found at all 4 sites and >20% were found only at 1 site. Trapping success of researchers and densities of small mammals varied greatly between sites. Although number of species increased with research effort, the most extensively studied site did not encompass all mammalian diversity in the region. To obtain a representative mammalian inventory, effort should focus on sampling mammalian fauna at multiple sites, rather than increasing time at 1 site.
Southern flying squirrels (Glaucomys volans) are small sciurid rodents that reside in deciduous forests of eastern North America. G. volans consumes primarily seeds and fruits, and is active year-round. During winter when food is sparse, flying squirrels conserve energy by forming aggregations in nest-lined cavities of trees. We compared seasonal changes in resting metabolic rate (RMR), nonshivering thermogenesis (NST), body temperature, and body mass of G. volans nesting communally residing in an outdoor enclosure to squirrels nesting singly housed in an outdoor laboratory. Flying squirrels were tested monthly from November 1997 to November 1998. Average RMR was highest in winter (1.14 ml O2 g−1 h−1) and lowest in summer (0.73 ml O2 g−1 h−1); minimal differences occurred among group and solitary nesters. Average RMR ranged from 33% (single) to 38% (communal) lower than predicted by body mass. Average NST was lowest in summer (1.62 ml O2 g−1 h−1) and peaked in winter (4.70 ml O2 g−1 h−1), demonstrating an inverse correlation with minimum ambient temperature. Squirrels nesting singly experienced a longer period of elevated NST in winter and higher mean NST year-round than did squirrels nesting communally. Average body mass ranged from a low of 66.9 g in September for both groups to a high of 76.4 g in communal nesters in December and 79.3 g for single nesters in March; average body temperature ranged from 36.3 to 38.9°C (communal nesters, December and May, respectively).
Although molecular evolution often appears to proceed in a clocklike fashion, examples to the contrary are increasing in number. Our study compares rate of cytochrome-b evolution in 21 rodent species, each of which belongs to a different genus. In these comparisons, substitutions at synonymous sites appear to be saturated, precluding inferences about rate of synonymous substitution. Rate of nonsynonymous substitution differs significantly among many of the rodents studied. However, the cause or causes of these differences in substitution rate remains in question. Differences in generation time, body size, or metabolic rate do not seem to be associated with rate of nonsynonymous substitution in these rodents. Effective population size remains a viable explanation of the observed rate heterogeneity. However, we suggest that a search for simple causes of differences in rate of molecular evolution may be difficult in light of numerous aspects of an organism's biology that may together influence evolutionary rates over space and time.
Phylogenetic relationships among 7 species of Reithrodontomys were examined using the complete mitochondrial cytochrome-b gene. DNA-sequence data were analyzed using parsimony (weighted and unweighted) and genetic distance methods. In all analyses, R. sumichrasti, R. megalotis, and R. zacatecae formed a monophyletic clade. Likewise, R. montanus and R. raviventris were depicted as sister taxa in all analyses. Our study supports recognition of R. zacatecae as a species distinct from R. megalotis and recognition of R. raviventris as distinct from R. montanus. Patterns of chromosomal evolution were examined using differential staining as resolved by 3 DNA probes and fluorescent in situ hybridization. Using the phylogeny based on DNA sequences, we concluded that there has been extensive chromosomal repatterning (in most cases karyotypic megaevolution) in the evolution of R. zacatecae, R. megalotis, R. sumichrasti, R. montanus, R. raviventris, and R. humulis.
Phylogenetic relationships of 6 species of the genus Akodon have been determined by mtDNA sequence analysis of the cytochrome-b gene, with the majority of specimens also identified by karyotype. We used maximum parsimony and distance analyses of 54 sequences to assess phylogenetic relationships and minimum spanning trees to compare genetic and geographic relationships among populations. The genus Bolomys was used as the outgroup. Akodon cursor, A. aff. cursor, and A. montensis, 3 morphologically cryptic but karyotypically different species of the cursor complex, each formed reciprocally monophyletic lineages. Twenty-one haplotypes were present in 23 individuals of A. cursor, and each of the 16 specimens of A. montensis had a unique haplotype. Within species, populations of A. cursor (19 localities) showed high variation with little geographic pattern. Distant populations (∼750 km apart, differing by 12 nucleotides) exhibited similar levels of differentiation as did geographically close populations (∼150 km apart, differing by 17 nucleotides). In contrast, A. montensis (12 localities) was structured geographically and exhibited a pattern consistent with an isolation-by-distance model of differentiation. Among other species in southeastern Brazil, A. mystax was related most closely to the cursor species complex, A. lindberghi was somewhat more distant, and A. serrensis was quite distinct.
Studies on Thomomys and Peromyscus, among others, have confirmed that karyotypic variation in mammals is often reflected in genome size variation. We used flow cytometry to estimate genome sizes from 91 individuals of the karyotypically variable Graomys griseoflavus complex from Argentina. Our samples represented 16 populations and included 2 ostensibly reproductively isolated forms. The mean genome size (2C value) for all populations, 5.72 pg ± 0.34 SD of DNA, was low for mammals, and the range was greater than observed in previous studies on Geomys, Thomomys, and bats. Two groups of populations were identified that differed in mean genome size. A high–genome-size group consisted of 2 populations in San Juan Province with a mean genome size of 7.38 ± 0.53 pg. These populations occupied the most arid part of the Monte Desert. A small–genome-size group included the remaining 14 populations that mostly occupied a broadly distributed, continuous habitat and possessed lower genome sizes with a mean of 5.62 ± 0.56 pg. Population means in this group ranged from 2C = 4.97 to 6.51. Previous studies have shown the existence of 2 reproductively isolated and karyotypically differentiated species within the G. griseoflavus complex. The high–genome-size group seems to correspond to the species with 2n = 42 (G. centralis) and the low–genome-size group to the species with 2n = 36–38 (G. griseoflavus). Flow cytometry is a potentially useful method to rapidly assess differentiation among populations of the G. griseoflavus complex.
Proechimys roberti has been considered an isolate representative of the guyannensis group of species of the genus Proechimys in the Cerrado of central Brazil, or regarded as a member of the longicaudatus group of species. We present new karyologic, morphometric, morphologic, and molecular data from populations spanning the gap between the previously known isolated distribution of P. roberti and the core distribution of the guyannensis group. All specimens had the same basic karyotype, 2n = 30, with fundamental number (FN) = 54–55. FN variation was due to a pericentric inversion affecting a small autosomal pair. Specimens from the eastern Amazon Basin and the Cerrado did not have any differentiation in external, cranial, and dental characters. In contrast, samples showed a significant multivariate morphometric variation, with a high heterogeneity among all populations, independent of Cerrado or Amazon location. Our results, coupled with phylogenetic analysis of cytochrome-b sequences, indicate that P. roberti is a valid species of the guyannensis group and that the species of this group occurring in eastern Amazon, P. oris, is probably a junior synonym of P. roberti.
To clarify population structure of finless porpoises (Neophocaena phocaenoides) in Japan, we examined mitochondrial DNA sequences of 174 animals. All individuals except for a female were collected in 5 geographically discrete coastal waters where Japanese porpoises are mainly distributed: Sendai Bay–Tokyo Bay, Ise–Mikawa Bays, Inland Sea–Hibiki Nada, Omura Bay, and Ariake Sound–Tachibana Bay. We analyzed 345 base pairs of the control region for all animals and detected 10 haplotypes. Two of those were shared by animals from > 1 area, whereas the other 8 were each found only in 1 area. The most common haplotype in Ise–Mikawa Bays and Ariake Sound–Tachibana Bay was not found at other locations. Analysis of the frequency distribution of haplotypes quantified genetic differentiation, and measurements of gene flow indicated limited dispersal of animals among locations. We conclude that finless porpoises in each of the 5 locations belong to distinct populations.
Taxonomic position of Otonycteris hemprichii always has been uncertain, although traditionally it has been considered closely related to Nycticeius, Rhogeessa, and Scotophilus in the tribe Nycticeini (Chiroptera: Vespertilionidae). A recent reevaluation of morphologic and karyotypic data alternatively placed Otonycteris in the tribe Plecotini with Barbastella, Corynorhinus, Euderma, Idionycteris, and Plecotus. We assessed taxonomic position of Otonycteris by analyzing a broad taxonomic sample, including nycticeine, plecotine, and antrozoine bats. Parsimony analysis of DNA sequences from about 2.7 kilobases of the mitochondrial genome (12S rRNA, tRNAVal, 16S rRNA) indicated that Otonycteris is related more closely to Antrozous and Rhogeessa than to any traditional plecotines. The analysis also supported monophyly for traditional plecotines. Not all relationships were resolved within the plecotines, but analysis corroborated previous studies in the sister relationship between Idionycteris and Euderma and monophyly of the Old World genus Plecotus and the New World genus Corynorhinus. Our phylogeny contradicts the most recent assessment of plecotine bats but is congruent with much of the available morphologic and karyotypic data on relationships within and among nycticeine and plecotine bats.
Qualitative and quantitative variation in morphology was assessed for 6 species of Myotis from South America to determine which taxa occur in Paraguay, characteristics that allow for their discrimination, and the degree of geographic and secondary sexual variation that occurs in Paraguayan forms. Secondary sexual dimorphism and geographic variation were evaluated from univariate and multivariate perspectives. Multivariate morphometric differences in cranial morphology among taxa, independent of size, and mensural characters that best separate species were determined using principal components analysis followed by size-adjusted discriminant function analysis. Five species, M. albescens, M. nigricans, M. riparius, M. ruber, and M. simus, occur in Paraguay and can be distinguished using combinations of cranial and external characteristics. No significant sexual dimorphism or geographic variation was detected in these taxa of Myotis in Paraguay. M. levis has not been recorded for Paraguay as previously reported, but it may occur in the country. M. simus, a species previously considered to be restricted to the Amazon Basin, occurs as far south as Paraguay and northern Argentina. Although M. simus varies significantly in size across its range, highly differentiated cranial and external morphology allows for recognition of this species across its range.
The short-nosed fruit bat, Cynopterus sphinx (Megachiroptera: Pteropodidae), is a common plant-visiting bat that is widely distributed throughout the Indomalayan region. We quantified foraging behavior of C. sphinx as individuals fed on fruits of Annona squamosa, leaves of Cassia fistula and Mimusops elengi, and fruits and leaves of Coccinia indica. After making several circling flights and engaging in brief hovering bouts, bats typically land directly on a single fruit and remove all or part of it with the mouth. In contrast, individuals remove leaves from trees during flight, without landing or hovering. C. sphinx typically transports fruits and leaves to feeding roosts where it extracts soluble contents and expels fibrous spats beneath day and feeding roosts. This bat consumes mostly fruits upon emergence from day roosts and feeds on leaves later in the night. These temporal differences in nightly foraging behavior may reflect the higher water and carbohydrate (energy) contents of fruits, compared with leaves, and help sustain flight activity throughout the night.
Availability of bridge roosts is a poorly understood but possibly important component underlying abundance and distribution of the potentially threatened bat Corynorhinus rafinesquii. We analyzed structural characteristics and surrounding habitat of 81 bridges in west-central Louisiana forests to determine which attributes of bridges influenced the selection of roosts by C. rafinesquii. Type of support structure under bridges, material with which bridges were built, proportion of surrounding habitat composed of mature deciduous forest, and road surface of bridges were significantly associated with selection of roost sites. On average, bats tagged with radiotransmitters roosted under bridges 50% of the time and in black gum trees (Nyssa sylvatica) 50% of the time. Preservation of bridges with beam supports and conservation of mature deciduous forest are likely to be important for maintaining populations of C. rafinesquii.
To determine characteristics associated with winter hibernacula of the eastern pipistrelle (Pipistrellus subflavus), microclimate parameters, land-use, and densities of bats were recorded and compared among 4 study sites, associated with box culverts under Interstate Highway 45 in Texas. Presence of bats in hibernacula varied throughout the year. Selection of winter hibernacula in temperate regions may not be dependent on microclimate parameters alone. Minimum temperature was the only significant microclimate predictor of abundance of bats and reflected seasonal use of hibernacula during winter. Analyses of land-use data revealed a significant correlation between number of bats present at each roost and amount of agriculture and forest surrounding each site. Distance from the opening of the culvert to forest also was correlated with number of bats. Occupancy of hibernacula by the eastern pipistrelle was greatest for December and January, with males consistently appearing in higher ratios than females. Fidelity of bats to hibernacula was highly variable within and between seasons. Recaptures ranged from 14 to 73% during both seasons with 24% of the bats marked during the 1st season returning the following year.
Growth patterns that lead to sexual dimorphism in adults are not well quantified. We measured 49 skeletal dimensions in male and female Chinchilla lanigera from radiographs of growing individuals taken during 320 days. Measurements for each individual were fit with a nonlinear Gompertz equation to quantify growth patterns. Differences in Gompertz parameters between sexes were compared with a t-test. Most significant differences between sexes in growth and final size were in the pelvic girdle (which formed the birth canal) and viscerocranium. Sexual dimorphism in the viscerocranium may support the hypothesis that differences in use of ecological niche often causes sexual dimorphism where females are larger than males.
Postweaning development of the skull of Didelphis albiventris was studied in juveniles (3.5–8 months), subadults (7.5–9.5 months), and adults (>9.5 months). Analysis of allometry of 15 skull measurements was performed on a continuous growth series of 52–61 specimens to evaluate quantitative ontogenetic changes. Complex modifications occurred in cranial bones or regions such as the palate, processes for origin and attachment of jaw muscles, mandibular joint, frontal region, braincase, occipital bones, and petrosal. All measurements except zygomatic breadth were either positively or negatively allometric. Neurocranial components grew with strongly negative (<1) coefficients of allometry. Adult proportions of the masticatory apparatus arose from the counteraction of developmental trends; for example, the space for large temporal muscles was provided by isometric growth of the zygomatic breadth versus slower growth of the braincase. We interpret most of the postweaning developments as a function of the shift from milk suckling to active mastication.
The blind mole rat (Spalax ehrenbergi) is a solitary and aggressive subterranean rodent. Our study revealed the unique anatomical structure of reproductive glands, ejaculate, and spermatozoon of the male blind mole rat and the effect of testosterone on those glands. Unlike other rodents, only the prostate and Cowper's accessory sex glands are present, whereas coagulating gland, seminal vesicle, and preputial gland are absent. Three groups of male blind mole rats were examined: intact, injected, and castrated animals, and resulting differences in morphology of reproductive glands were examined histologically using quantitative measurements. Lowered testosterone levels in castrated blind mole rats caused a reduction in weight and star volume (υ*) of the prostate and Cowper's glands. Testosterone injection produced an increase in mass of the prostate gland but not in Cowper's glands, whereas both prostate tubuli υ* and Cowper's gland tubuli υ* also increased. The blind mole rat possesses only 2 accessory sex glands, both of which are influenced by testosterone levels.
Recent studies have suggested that the relatively large size of the vomeronasal neuroepithelium (VNNE) in the male mammal may be related inversely to the amount of parental care contributed. We tested this hypothesis using 2 species of Microtus that differ in reproductive strategies and in level of care of the offspring. We studied the nasal tissues of 8 male meadow voles (Microtus pennsylvanicus) and 8 male prairie voles (M. ochrogaster), captured between June and August, 1998. The heads were prepared histologically for serial sectioning at 10–16 μm, and stained with hematoxylin and eosin. Sections were examined by light microscopy, and the VNNE was quantified for each specimen using a computer 3-dimensional reconstruction technique. Receptor cells also were quantified with a Leica photomicroscope using an ocular grid calibrated by a stage micrometer. No (P > 0.05) differences occurred between species for length or volume of the VNNE when expressed as absolute measures or as ratios of somatic measures. No (P > 0.05) differences occurred in receptor population between species. Although testicular weight seemed to show a positive allometric relationship with body size, no such association was seen for VNNE measurements. Our results do not support the hypothesis that VNNE size is associated negatively with the level of parental care by male voles. Multiple factors may influence size of the VNNE in wild Microtus, which likely include an interaction of the genome, behavior, and environment.
Using light microscospy, cross sections of the superior vestibular nerve were compared in 2 tree-dwelling species of squirrels (Sciurus carolinensis and S. niger) and 3 ground-dwelling species (Spermophilus tridecemlineatus, S. mexicanus, and S. variegatus). Fiber number, internal minor diameter of the axon, and axon area were measured for 31,959 fibers taken from 5 males of each species. Significant differences were not found within or among species, suggesting that climbing behaviors are not correlated with these morphologic features of the superior vestibular nerve.
Bearded and ringed seals from Svalbard, Norway, often have strongly rust-colored faces; the fore-flippers also are rust-colored in some animals. Element analyses of fur from normally colored and rust-colored seals of both species showed that high concentrations of iron were present in the colored fur, indicating that iron oxides are probably the main reason for the unnatural coloration. High concentrations of vanadium and manganese also were found in samples of colored fur. Oxides of these elements also may contribute to the discoloration. We suggest that seals acquire elements responsible for the coloration while feeding in soft-bottom sediments. Their faces and flippers make contact with rich deposits of iron monosulfide in a reducing environment. When this sediment is brought up into the water column by the seals, the iron monosulfide is oxidized to form iron oxides that precipitate onto the hair shafts of the seals. The higher incidence of rust-colored bearded seals, compared with ringed seals, is explained by the greater dependence of the former species on benthic prey items.
We examined data from 3,743 buffalo (Syncerus caffer) culled between 1991 and 1998 in Kruger National Park, South Africa, to evaluate effects of bovine tuberculosis on the buffalo population and examine risk factors of bovine tuberculosis. We found no evidence that bovine tuberculosis affected fertility or lactation status of female buffalo, but adult buffalo >3 years old were underrepresented in infected herds. Logistic regression analysis demonstrated that older buffalo were at greater risk for bovine tuberculosis than younger buffalo and risk of acquiring bovine tuberculosis increased for all age groups as prevalence in the herd increased.
Blood serum was collected between June 1990 and August 1992 from newborn white-tailed deer (Odocoileus virginianus) fitted with radiocollars. We measured serum concentrations of immunoreactive tumor necrosis factor-α (iTNF-α) and immunoreactive interleukin-6 (iIL-6) to relate cytokine expression to probability of mortality during the first 21 days of life. Stepwise logistic regression indicated that iTNF-α, hemolytic complement, gamma globulins, gamma glutamyl transferase, and mass/length3 could predict survival of white-tailed deer during the first 21 days of life with 90.9% accuracy. Univariate logistic regression did not show a relationship between serum concentrations of iTNF-α or iIL-6 and probability of mortality. However, fawns that died before 21 days of age tended to have greater levels of iTNF-α (688.4 ± 168.8 pg/ml) than survivors (412.9 ± 81.2 pg/ml). Although these data suggest that iTNF-α may be a useful predictor of stress, additional research is needed to understand response of cytokines to neonatal stress and mortality and to elucidate their utility as indices.
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